Eur J Clin Microbiol Infect Dis DOI 10.1007/s10096-017-2917-8

ORIGINAL ARTICLE

Burden of fungal infections in

M. Chekiri-Talbi1 & D. W. Denning2

Received: 21 December 2016 /Accepted: 21 December 2016 # Springer-Verlag Berlin Heidelberg 2017

Abstract We report for the first time in Algeria and provide Introduction burden estimates. We searched for existing data and estimated the incidence and prevalence of fungal diseases based on the Algeria is Africa’s biggest country by land area, and is population at risk and available epidemiological data. the world’s 10th largest. The health system in Algeria is Demographic data were derived from the National Office of designed to take care of the health needs of the popula- Statistics (Office National des Statistiques: ONS), World tion for all problems with free access to care. It is deliv- Health Organization (WHO), The Joint Nations Programme ered by the State, at national and regional levels [1].The on HIV/AIDS (UNAIDS) and national published reports. life expectancy in men is 72 years and in women When no data existed, risk populations were used to estimate 75 years. Twenty-eight percent of Algeria’s population frequencies of fungal infections, using previously described is under 16 years old [2] and health policy focuses on methodology. Algeria has 40.4 million inhabitants, and prob- preventative health care, including immunization [3]. ably at least 568,900 (1.41%) of Algerians have a serious There are issues around sanitation and clean water for fungal infection each year. Recurrent vulvovaginal candidiasis all, and communicable and waterborne diseases are rela- (485,000) and fungal asthma (72,000) are probably the tively common. commonest problems, as there are over 1 million adult asth- There has been very little focus on fungal diseases, matics. Candidaemia is estimated in 2,020 people, invasive with the notable exception of cutaneous infections. aspergillosis in 2,865 people, and intra-abdominal candidiasis More recently, increased focus on hospital-acquired fun- in 303 people; these are the most common life-threatening gal disease has emerged with cases and series of problems. AIDS is uncommon, but cancer is not (45,000 Candida biofilm formation [4]aswellassomedeep new cases of cancer including 1,500 in children), nor is mycoses [5] aspergillosis [6], cryptococcosis [7], COPD (an estimated 317,762 patients, of whom 20.3% are candidemia [8], mycetoma [9] and sporotrichosis ; given admitted to hospital each year). A focus on improving the this poverty of data, we have attempted to estimate the diagnosis and epidemiological data related to fungal infection burden of fungal diseases in Algeria, using previously is necessary in Algeria. published methodology based on populations at risk and local incidence and prevalence data (Table 1).

* M. Chekiri-Talbi Methods [email protected] We searched for existing data, and estimated the inci- 1 Pharmacy Department, Université Saad Dahlab de , dence and prevalence of fungal diseases based on the Blida 09000, Algeria population at risk and available epidemiological data. 2 The University of Manchester, National Aspergillosis Centre, Demographic data were derived from the National University Hospital of South Manchester and Manchester Academic Office of Statistics (ONS), World Health Organization Health Science Centre, Manchester, UK (WHO), The United Nations Programme on HIV/AIDS Eur J Clin Microbiol Infect Dis

Table 1 Prevalence rates presented used to estimate the Number Source burden of serious fungal diseases in Algeria Population Population data [10] Population (M) 40,400,000 [10] %children 28 [10] Number of children 11,312,000 [10] Adults 29,088,000 [10] % women over 60 7 [10] Respiratory diseases Pulmonary tuberculosis annual incidence total 5,418 [11] Population over 40 years 11,312,522 [11] COPD prevalence all GOLD stages 9.20% [12] Asthma rate in adults 3.10% [13] Asthma numbers in adults 1 ,252,400 [13] HIV/AIDS patients Current total HIV/AIDS 9,103 [14] Proportion of diagnosed cases on ARVs 1,561 [14] Number of diagnosed cases not receiving ARVs 7,542 [14] Annual new AIDS cases (at risk of OIs) 1,077 [14] AIDS-related deaths in 2014 843 [14] AML patients per year 300 [15] Renal Tx per year 200 [16]

(UNAIDS) and national published reports .Estimated Results and discussion HIV patient numbers were derived from the UNAIDS 2014 data. Patients with acute myeloid leukaemia were Superficial mycoses and dermatophytic infection assumed to be about 300 annually [15]. We identified 170 to 200 renal transplantation procedures annually In Algeria, onychomycosis and tinea capitis dominate the [16], and no other transplant procedures. The prevalence superficial mycoses [21]. Trichophyton rubrum is the pre- of chronic obstructive pulmonary disease (COPD) is dominant pathogen of feet and the inguinal folds [21]. 9.2% in the over-40-year-old population [12], and we Tinea capitis represents a public health problem in have assumed that 10.5% are admitted to hospital each Algeria, despite improvement of living conditions and af- year [17]. The proportion of adults and children with fects mostly children of school age [22]. Ectothrix tinea is clinical asthma is 3.1% and 4.1% respectively, and we the most observed form of tinea capitis. T.mentagrophytes have used only the adult figure for estimates (http:// is primarily responsible for inflammatory disease (kerion www.liberte-algerie.com/radar/un-million-dasthmatiques- celsi and related conditions) [23].There has been a rise in recenses-en-algerie-201363)[13].There are at least 100 Microsporum audouinii anthropophilic species, especially cases of cystic fibrosis cases in Algeria [18] but we in the north [24]. have not included these in our estimates. Pulmonary Using the published example of Constantine which has tuberculosis (TB) burden was taken from the Société a population of 950,000, and assuming that tinea capitis Algérienne de Pneumo-Phtisiologie (SAPP) [11], and only occurs in children (95%) [20, 25]thentheratewould 10% are assumed to have died. be 37.7/100,000. Nationally, this equates to 4,265 cases Amongst cutaneous infections, tinea capitis comes second annually. This is almost certainly a significant underesti- after onychomycosis in frequency in dermatology practice mate, as local surveys of school children indicate higher [19]. We found one published estimate of annual incidence; frequencies, but are not systematic and so not in the Constantine area, ∼100 new cases were seen to be di- extrapolatable. Published studies found variable preva- agnosed annually (2007–2011) [20]. In estimating the mini- lence from region to region: (24.6%) [23], mal national burden, we have assumed that all cases are seen Constantine (37.2%) [21], Tipaza (62.4%) [23, 26], and at the University Hospital for the entire region, and that this Blida (66.4%) [27]. We note that tinea capitis is more frequency is reflected nationwide. When no data existed, risk important in these last Wilayas (localities), possibly ex- populations were used to estimate frequencies of fungal infec- plained by their more rural populations. tions, using methodology described by LIFE. We have sum- Our data are similar to other countries in north Africa in- marized all recent published papers about mycoses in Algeria. cluding Tunisia and , where M.canis and Eur J Clin Microbiol Infect Dis

T.violaceum are the commonest agents of tinea capitis [26, Egypt, fungi are responsible for 28–55% of cases of microbial 28]. While favus (definitive tinea capitis usually caused by keratitis [36]. Trichophyton schoenleinii) is rarely diagnosed in Algeria [29] (in the south only) [30], this pathology is still frequent in Tunisia and Morocco [26, 28]. Invasive mycoses Dermatophytes are also often isolated from ear infec- tions, with the predominant species being M.canis, Invasive aspergillosis T.rubrum, T.violaceum ,andT.mentagrophytes [31]. In Algeria, Aspergillus otitis is more often caused by In the lung, the incidence of invasive aspergillosis in the neutro- A. niger, A. flavus ,andA. terreus [30, 32]. penic patient in the north of the country is 7.7%, diagnosed by Vulvovaginal candidiasis (VVC) is common in women, antigen detection with ELISA [6]; sixteen of 208 neutropenic but there are no published data from Algeria. Candida patientswerepositive,andall16diedfromprogressiveleukemia. albicans is commonly seen microscopically in vaginal No special environmental precautions were in place. Aspergillus smears and cultured. We have attempted an estimate of flavus and Aspergillus niger were more frequent than Aspergillus the prevalence of recurrent VVC (>4 episodes annually), fumigatus in the local environment of the patient [6]. In Tunisia, based on data from five countries in Europe (including A.flavus also is more often isolated than A. fumigatus [37, 38]. ) and the USA [33]. Women over-diagnose VVC Therefore, we anticipate 47 cases of IA in haematological pa- themselves, as other problems are common mimics, nota- tients and renal transplant recipients annually. bly bacterial vaginosis. We have therefore reduced the self- COPD is relatively common in Algeria, with an estimated reported rate of recurrent VVC (rVVC) obtained by an prevalence of 1,040,000 patients [39]. Of these, 20.3% are internet survey from 9% to 6% in 15- to 50-year-old wom- admitted to hospital each year [40]. Assuming the rate of en [33, 34]. However a remarkable 485,188 women prob- invasive aspergillosis is the same as in Madrid [41]basedon ably suffer with rVVC in any given year, a population rate culture alone at 1.3%, an estimated 2,747 patients with COPD of 2,402/100,000 among females (Table 2). This fungal will develop invasive aspergillosis each year. problem dwarfs all others. There are an estimated 2,707 cases of lung cancer diag- Fungal keratitis is rarely diagnosed in Algeria, and may be nosed each year in Algeria, 7.1% of all cancers [42]. The rate missed. The causative agents are Candida albicans,followed of invasive aspergillosis in such patients was documented by by filamentous fungi [35]. There are no population estimates Yan et al. [40], in Chengdu in China at 2.6%, and if this rate in Algeria, but in Egypt, with a population about twice that of also pertains to Algeria, then 71 IA cases are likely. Clearly Algeria, there are an estimated 11,550 cases annually. In this needs local confirmation.

Table 2 Estimated burden of invasive (annual incidence) and chronic and allergic (prevalence) fungal diseases in Algeria

Infection Number of infections per underlying disorder /year Total Rate burden /100 K None HIV/AIDS Respiratory Cancer/ ICU Tx

Oesophageal candidiasis 832 832 2.1 Candidaemia 1,414 606 2,020 5.0 Intra-abdominal candidiasis 303 303 0.75 Recurrent vaginal candidiasis >4 times/year 485,188 485,188 2,402 Allergic broncho-pulmonary aspergillosis (ABPA) 31,310 31,310 77 Severe asthma with fungal sensitisation (SAFS) 41,329 41,329 102 Chronic pulmonary aspergillosis (CPA) 897 897 2.2 Invasive aspergillosis 2,818 47 2,865 7.1 Mucormycosis 79 79 0.2 Cryptococcalmeningitis 28 7 36 0.09 Pneumocystis pneumonia 74 74 0.18 Tinea capitis 4,265 4,265 10.6 Total burden estimated 568,942 Eur J Clin Microbiol Infect Dis

Cryptococcal meningitis Tuberculosis was the most common underlying diagnosis (79.4%) [11]. Based on the 5,418 survivors of pulmonary In a recent retrospective laboratory study, 24 of 425 HIV pa- TB in 2014 in Algeria, we estimate that 228 new patients will tients had cryptococosis from January 2002 to March 2015. develop CPA annually (incidence) and that the 5-year preva- The incidence was 5.6%, translating into one to four cases per lence is about 717 cases, assuming a 15% annual mortality or year [43].Of the 24 patients, 18 (75%) were HIV seropositive, surgical resection. Assuming that 80% of the cases follow and so we have assumed that 25% of cryptococcosis cases in tuberculosis based on the series above, there are about 900 Algeria are not HIV-related, as also described in four patients. patients with CPA in Algeria (2.2/100,000). This high proportion was also found in another study, where Among adults in Algeria, 3.1% have clinical asthma, or 60 of 77 (78%) patients with cryptoccocosis were HIV posi- 1,252,400 patients [51]. If we assume that the rate of allergic tive [44]. Cryptococcosis may be sometimes seen in non-HIV broncho-pulmonary aspergillosis (ABPA) is the same as in patients, but this is probably rare [7]. SaudiArabiaat2.5%,andthatthisratepertainstothewhole To estimate burden, we have assumed a 7-year linear decline population, not just those seen in secondary care, we estimate in CD4 count to <200 × 106/l and therefore anticipate the risk 31,310 people have ABPA. Taking only the most severe group populationfor opportunistic infectionstobeabout 500 patients. of asthmatics (10%), fungal sensitisation is likely to be similar Assuming a 5.6% cryptococcal rate and a 15% PCP rate (mean to other countries with rising rates as asthma severity in- of many international studies) [45], we estimate about 28 HIV- creases. If we assume that this is 33%, then 3% of the adult associated cases of cryptococcosis, seven non-HIV cases, and asthmatics have severe asthma with fungal sensitisation about 74 patients with PCP and AIDS each year. (SAFS), or 41,329 people. They may be some duplication between ABPA and SAFS, because sensitization to Candidemia Aspergillus is universal in ABPA, and some of these patients have severe asthma. Yeasts in blood are a major cause of morbidity and mortality, and are frequently associated with the implantation of vascular catheters, especially in immunocompromised patients. We Conclusion have estimated a 5/100,000 rate in accord with other European countries, in the absence of local epidemiology da- In Algeria, there are many superficial mycoses, especially ta, a total of 2,020 cases. Candida spp. are most frequent, but onychomycosis and tinea capitis. Under-recognised problems species distribution is variable from one study to another. In include recurrent VVC in women, fungal keratitis, chronic Algiers, 65 of 463 positive blood cultures (14.1%) grew pulmonary and allergic aspergillosis, and all serious deep my- Candida, primarily Candida parapsilosis (36.6%), then coses. There are extremely few data on Invasive filamentous C. albicans (31.6%), C. tropicalis (23.3%), C. krusei (3.3%), fungal infections, yet they are likely to be frequent in immu- and finally C. lusitaniae (1.6%) [5]. 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